Geobiology. 2018;16:341–352. wileyonlinelibrary.com/journal/gbi  | 341© 2018 John Wiley & Sons Ltd

Received:16July2017  |  Accepted:31March2018DOI: 10.1111/gbi.12289

O R I G I N A L A R T I C L E

Tracking the rise of eukaryotes to ecological dominance with zinc isotopes

Terry T. Isson1  | Gordon D. Love2 | Christopher L. Dupont3 | Christopher T. Reinhard4 |  Alex J. Zumberge2 | Dan Asael1 | Bleuenn Gueguen5 | John McCrow6 | Ben C. Gill7 |  Jeremy Owens8 | Robert H. Rainbird9 | Alan D. Rooney1  | Ming-Yu Zhao1 |  Eva E. Stueeken10  | Kurt O. Konhauser11 | Seth G. John12 | Timothy W. Lyons2 |  Noah J. Planavsky1

1GeologyandGeophysics,YaleUniversity,NewHaven,Connecticut2EarthScience,UniversityofCalifornia,Riverside,Riverside,California3MicrobialandEnvironmentalGenomics,J.CraigVenterInstitute,SanDiego,California4GeorgiaInstituteofTechnology,Atlanta,Georgia5EarthScience,UniversitédeBretagneOccidentale,Brest,France6J.CraigVenterInstitute,Rockville,Maryland7Geosciences,VirginiaTech,Blacksburg,Virginia8FloridaStateUniversity,Tallahassee,Florida9Geology,GeologicalSurveyofCanada,Ottawa,ON,Canada10SchoolofEarthandEnvironmentalSciences,UniversityofStAndrews,StAndrews,Scotland,UK11EarthandAtmosphericSciences,UniversityofAlberta,Edmonton,AB,Canada12EarthScience,UniversityofSouthernCarolina,LosAngeles,California

CorrespondenceTerryT.Isson,YaleUniversity,NewHaven,CT.Email:terry.t.isson@gmail.com

Funding informationNSFFESDProgram;NASAAstrobiologyInstitute

AbstractThebiogeochemicalcyclingofzinc(Zn)isintimatelycoupledwithorganiccarbonintheocean.BasedonanextensivenewsedimentaryZnisotoperecordacrossEarth’shistory,weprovideevidenceforafundamentalshiftinthemarineZncycle~800mil-lionyearsago.Wediscussawiderangeofpotentialdriversforthistransitionandproposethat,withinavailableconstraints,a restructuringofmarineecosystems isthemostparsimoniousexplanationforthisshift.Usingaglobalisotopemassbalanceapproach,weshowthatachangeintheorganicZn/CratioisrequiredtoaccountforobservedZnisotopetrendsthroughtime.GiventhehigheraffinityofeukaryotesforZn relative to prokaryotes,we suggest that a shift toward amore eukaryote-richecosystemcouldhaveprovidedameansofmoreefficientlysequesteringorganic-derivedZn.Despite themuchearlier appearanceof eukaryotes in themicrofossilrecord(~1700to1600millionyearsago),ourdatasuggestadelayedrisetoecologicalprominence during the Neoproterozoic, consistent with the currently acceptedorganicbiomarkerrecords.

K E Y W O R D S

carboncycle,Earthhistory,eukaryotes,marineproductivity,oceanchemistry,zinc,zincisotopes

342  |     ISSON et al.

1  | INTRODUC TION

Whileeukaryoticmicroalgaeareresponsibleforasubstantialportionof marine export production today (Falkowski etal., 2004), primaryproductionandmicrobialcommunitiesintheArcheanandProterozoicoceansaretraditionallyviewedtohavebeendominatedbyunicellularprokaryotes(Brocksetal.,2017;Butterfield,2015;Knoll,2014).Thislong-termshifttowardamoreeukaryote-richEarthsystemhasbeenmechanistically linked to numerous major events in Earth’s history,in particular the onset of low-latitude “Snowball Earth” glaciations,majorcarboncycleperturbations,andocean-atmosphereoxygenationduringNeoproterozoictime(e.g.,Feulner,Hallmann,&Kienert,2015;Tziperman,Halevy,Johnston,Knoll,&Schrag,2011;Zhuetal.,2016).However,althoughithasbeencommonlyproposedthattherewasamajorecosystemshiftduringtheNeoproterozoic,therearerelativelyfewconstraintsoneithertheextentofmarineproductivityorthecom-positionofplanktoncommunitiesthroughmostofEarth’shistory.

Thus far, twomainapproacheshavebeenapplied to track theearly evolution of primary producers. The microfossil record hasbeenusedbothtodelineatetheappearanceoftheearliestdefini-tiveeukaryotesat~1700–1600Ma(Butterfield,2015;Knoll,Javaux,Hewitt,&Cohen, 2006) and to track theonset of extensive algalprimaryproductivityby~800Ma(Brocksetal.,2017;Feulneretal.,2015;Knoll,2014).Molecularfossils(organicbiomarkers)havealsobeenusedtotracktheevolutionofphototrophsandthebalanceofbacterialversusalgalproductivity.Forexample,theratioofhopane(e.g.,bacterial)tosterane(e.g.,eukaryotic)biomarkerscanpotentiallyprovideafirst-orderviewoftherelativebalancebetweenbacterialand eukaryotic inputs in aquatic depositional settings (Figure1).While there have been numerous reports of abundant eukaryoticbiomarkers inMesoproterozoic rocks (e.g., Zhang etal., 2016), re-centlipidbiomarkerevidence,usingcleananalyticalmethodologiestominimizecontamination,suggeststhattheearliestdetectableandrobusteukaryotic (24-alkylated) steranebiomarkers appear some-timewithin theNeoproterozoicEra (<1000Ma) (e.g.,Brocksetal.,2015,2017;Frenchetal.,2015;Loveetal.,2009)(seeAppendixS1).Earlier reports of abundant steranes, as old as 2700Ma, are now

attributable to contamination artifacts (French etal., 2015).Here,weproposeanoveltracerforshiftsinmarineecosystemstructure—thatis,acoupledrecordofthephase-specificsedimentaryenrich-mentandstableisotopecompositionofzinc(Zn).

2  | THE BIOLOGIC AL USE OF ZINC

StableisotopesofZnhavethepotentialtotracktheriseandecologicalexpansionofeukaryotesintheglobalocean.Whileallorganismsuti-lizeZn,moderneukaryoticphytoplanktonappeartohaveelevatedZndemandsandelevatedZn/Cratiosrelativetocyanobacteria(Nuester,Vogt,Newville,Kustka,&Twining,2012;Quigg,Irwin,&Finkel,2011;Twining,Baines,&Fisher,2004;Twiningetal.,2003,2011). Inaddi-tion,culturesshowthatZncanbecolimitingforeukaryoticalgae(e.g.,Zn-C and Zn-P colimitation) (Brand, Sunda, & Guillard, 1983; John,Geis, Saito, & Boyle, 2007; Morel etal., 1994; Schulz etal., 2004;Shaked,Xu,Leblanc,&Morel,2006;Sunda&Huntsman,1992,1995).Specifically,reducedgrowthrateshavebeenshowninmultiple(>25)eukaryoticphytoplanktonspeciesatfreeZn2+concentrationsbelow10−11.5Mwhileothermoretolerantspeciesonlyexhibitadeclinestart-ingat10−13M(Anderson,Morel,&Guillard,1978;Brandetal.,1983;Ellwood&Hunter,2000;Johnetal.,2007;Moreletal.,1994;Schulzetal.,2004;Shakedetal.,2006;Sunda&Huntsman,1992,1995,1998,2005;Tortell&Price,1996).Inmoredetailedstudies,lowinorganicZnconcentrationshavebeendemonstratedtoreducetheactivitiesofkeyspecificZnmetalloenzymesdramatically,suchascarbonicanhydrase,whichfacilitatestheacquisitionofbicarbonate(Moreletal.,1994),andalkaline phosphatase, which allows phytoplankton to acquire phos-phorousfromorganicphosphoruscompounds(Shakedetal.,2006).Insomeregionsoftheocean(e.g.,areasofhighnutrientandlowchloro-phyll)Znadditioncanresultinincreasedgrowthrates(Chappelletal.,2016; Coale, 1991; Franck, Bruland, Hutchins, & Brzezinski, 2003;Jakuba,Saito,Moffett,&Xu,2012). Inaddition, insomecases,sub-tlechangesinphytoplanktoncomposition(ecosystemstructure)havebeenobservedwiththeadditionofZn(Crawfordetal.,2003;Leblancetal.,2005;Lohan,Crawford,Purdie,&Statham,2005).

F IGURE  1 Organicbiomarkerrecorddepictingthepresence/absenceofeukaryoticsteranesinProterozoicorganic-richshales[Colourfigurecanbeviewedatwileyonlinelibrary.com]

Barney Creek Fm.N. Australia [1]

Xiamaling Fm.N. China [4]

Hongshuizhuang Fm.N. China [13]

Taoudeni BasinTouirist Fm. (Atar Gp.)NW Africa [5,17]

Chuar Gp.Laurentia [6,14,15,19]

Visingso Gp.Baltica [6,19]

McArthur BasinVelkerri Fm. (Roper Gp.)

N. Australia [2,3]

Malgina Fm.E. Siberia [16]

1,640 Time (Ma)1,370 1,100 7428001,000 8501,430 Phan.

abundant hopane biomarkers from bacteria; no steranes from eukaryotes

Stu

rtia

n

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inoa

n

24-ipcsterane/hopane ratio increases

Post-Sturtian to Early CambrianSiberia, Australia, Oman, India, et al.

[7,8,9,10,11,12,18-20]

[1] Brocks et al., 2005[2] Dutkiewicz, Volk, Ridley, & George, 2003[3] Flannery and George, 2014[4] Luo, Hallmann, Xie, Ruan, & Summons, 2015

[9] Mckirdy, Webster, Arouri, Grey, & Gostin, 2006[10] Love et al., 2009[11] Grosjean, Love, Stalvies, Fike, & Summons, 2009[12] Kelly, Love, Zumberge, & Summons, 2011

[5] Blumenberg, Thiel, Riegel, Kah, & Reitner, 2012[6] Brocks et al., 2015[7] Grantham, 1986[8] McCaffrey et al., 1994

[13] Luo, Ono, Beukes, Wang, Xie, & Summons, 2016 [14] Summons et al., 1988 [15] Vogel, Thorsen, Curry, Sandager, & Uldbjerg, 2005[16] Suslova, Parfenova, Saraev, & Nagovitsyn, 2017

[17] Gueneli, Brocks, & Legendre, 2012 [18] Bhattacharya, Dutta, & Summons, 2017[19] Brocks et al., 2017[20] Hoshino et al., 2017

Proterozoic biomarker recordEukaryotic primary productivity dominated by:

Red algal clades/heterotrophs

Green algal clade

     |  343ISSON et al.

In contrast, culture studies of cyanobacteria conducted thus farhavenotfoundZndemandssimilartothatobservedineukaryotes.InculturestudiesthecommonmarinecyanobacteriaProchlorococcus and SynechococcusappearnothaveresolvableZnrequirements,demon-stratinginvariantgrowthrateswhenZnisdepleted(Brandetal.,1983;Saito, Moffett, Chisholm, &Waterbury, 2002; Sunda & Huntsman,1995).However,ithasbeendiscoveredthatextantcyanobacteriaarenotentirelydevoidofZn.ForinstanceZn-carbonicanhydrasemetallo-enzymeshavebeenfoundtobeexpressedincyanobacteria(Blindauer,2008; So etal., 2004). Further,more recent culturework has high-lightedthepossibleuseofZninproteinsinvolvedinPO4

3−acquisitionwhen subject tophosphorousdeficiency (Cox&Saito, 2013)—likelylinkedtotheexpressionofextracellularphosphataseincyanobacteria(Bar-Yosef,Sukenik,Hadas,Viner-Mozzini,&Kaplan,2010;Whitton,Grainger,Hawley,&Simon,1991).Itisimportanttonotethatwithin-creasinglyelevatedambientZn levels,moreZncanbe incorporatedintocyanobacteria(Ohnemusetal.,2017).However,thishighuptakemaybeinadvertentanditisunlikelythattherehadeverbeenmarkedlyelevatedZnconcentrationsinsurfacewatersduetoZnsorption,up-take,andscavenging.Cyanobacteriaalsohaveahighercellularsurfaceareatovolumeratio(relativetoeukaryoticcells)thatfacilitateshigherdegrees of adsorption over assimilation, such that a cyanobacteria-dominatedecosystemisintheorycapableofforcingthesamedegreeofZndrawdowninsurfacewaterswithamuchlowerdegreeoforgan-ically incorporatedZn.Duringthistime, ironoxidescavengingcouldhavealsosignificantlyinfluencedwatercolumnZnprofiles.Therefore,althoughmorework is required, fieldstudiesandcultureworkbothstronglysupporttheobservationthatsubstantiallylessZnwillbein-corporated into biomass when cyanobacteria instead of eukaryoticphytoplanktonarethedominantprimaryproducers.

Genomicsurveysofgenesencodingformetalbindingproteinspro-videanadditionalmeanstoprobeZnrequirementsandtheevolution-aryhistoryofZnutilization.BasedonpredictedZnbindingproteinsfromwholegenomesequences,highZnrequirementsareobserved

for all major eukaryotic clades (Dupont, Butcher, Valas, Bourne, &Caetano-Anollés,2010;Dupont,Yang,Palenik,&Bourne,2006). Infact,ouranalysiswithupdatedgenomicdatabases(Figure2)suggeststhatZn isoftenthemostabundant inorganiccofactor ineukaryoticenzymesacrossalllineages.Further,eukaryoticgenomeshavesignifi-cantlymoreZnbindingproteinsthanprokaryotesasapercentageofthetotalpredictedproteome(Figure2a–b;seeAppendixS1).WefindthathighnumbersofgenesforZnbindingproteinsarenotonlyfoundinlaterevolvingcladesthatdominatemodernoceans,butalsoinsomeof the earliest evolving groups of eukaryotic algae, such as rhodo-phytes (Figure2c).DiverseuseofZn ineukaryotes isclearlyacon-servedandbasaltrait (Figure2c).AlthoughgenomicdatacannotbedirectlytranslatedintoZnquotas,thisworksupportsthepremisethatthereisafundamentaldifferencebetweeneukaryoticandprokaryoticZnutilizationandthatthisdifferencewouldhavebeenpresentinearlyevolvingeukaryotes.ContrastsinZnusagecanbelinkedtoanabun-danceofnucleus-localizedproteinsineukaryotes(e.g.,ZnfingersandRINGdomains)responsibleforDNA–RNAtranscriptionandprotein–proteininteractions(Berg&Shi,1996;Dupontetal.,2010;Rhodes&Klug,1993;Twiningetal.,2004).ThisrelationshipisconsistentwithobservationsfrommarineplanktonthatrevealZnlocalizationwithinthenuclei,ahallmarkfeatureofeukaryotes(Twining&Baines,2013;Twining, Baines,Vogt, Jonge,&Martin, 2008; Twining etal., 2003,2004).Insum,whole-cellZnmeasurementsandgenome-basedanaly-sessupporttheassertionthateukaryoticphytoplanktonhavesignifi-cantlyelevatedZnutilizationrelativetoprokaryoticphytoplankton.

3  | GLOBAL ZINC ISOTOPE MA SS BAL ANCE: ORGANIC BIOMA SS, A L ARGE AND ISOTOPIC ALLY LIGHT SINK FOR ZINC

The global mean δ66Zn value of modern seawater is ~0.5‰,while sourcesofZn to theoceans, including riverine, aerosol, and

F IGURE  2 Genomeencodedmetalutilization:Thepercentageofiron(red)andzinc(blue)bindingdomainscomparedwiththetotalnumberofproteindomainsindiscretegenomesof(a)cyanobacteria(n = 123)and(b)eukaryotes(n = 437).(c)Percentageofzinc-bindingdomainsineukaryoticandprokaryoticphytoplankton,relativetothetotalnumberofproteindomainsencodedbyeachgenome[Colourfigurecanbeviewedatwileyonlinelibrary.com]

0

5

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20

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30

0 2,000 4,000 6,000 8,000 10,000 12,000

Zinc Iron

0

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Chlorophytes Rhodophytes Haptophytes Bacillophytes Pelagophytes Cyanobacteria

Total No. of Domains Annotated

% b

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(a) Cyanobacteria (b) Eukaryotes (c) Zn and Phytoplankton

Zinc Iron

344  |     ISSON et al.

hydrothermalinputs,areclosetotheaveragecrustalvalueof~0.3‰(Little,Vance,Walker-Brown,&Landing,2014).IronandmanganeseoxidesscavengeisotopicallyheavyZn(Δ66Zn~0.3to0.5‰)(Bryan,Dong,Wilkes,&Wasylenki,2015;Little,Sherman,Vance,&Hein,2014;Maréchal, Nicolas, Douchet, & Albarède, 2000; Pokrovsky,Viers, & Freydier, 2005). Carbonates appear to be unfraction-ated from seawater; however, isotopically heavy carbonates havebeen observed within the geologic record (e.g., Pichat, Douchet,& Albarède, 2003).While we do not yet understand the specificcontrolsonZnincorporationintocarbonates(VanDijk,DeNooijer,Wolthers,&Reichart,2017),abinitioworksuggeststhattheisotopicsignatureofZnassociatedwithcarbonatespeciesoughttovarywithambientpHlevels(Fujii,Moynier,Blichert-Toft,&Albarède,2014).InthemostrecentsummaryoftheglobalisotopemassbalanceofZn,theisotopicallylightsinkwasnotfullyresolved(Little,Vance,etal.,2014),althoughorganic-richcontinentalmarginshavebeenshowntoburylightZn(Little,Vance,Mcmanus,&Severmann,2016).Here,webuildfrompreviousworkontheZnmassbalanceandnewdata

that constrain the isotopic composition of previously unidentifiedorganicandsulfidemarineexportfluxes(Figure3).WediscusseachofthemajorZnburialtermsandproposeabalancedmodernZniso-topebudget(Figures3and4).

Culture experiments reveal that eukaryotic phytoplanktonpreferentially incorporate the lighter isotopesofZnwithan iso-topicfractionation(Δ66Znorg-sw)between−0.8‰to−0.2‰(John&Conway,2014; Johnetal.,2007).Theway inwhichbiologicalfractionationsmanifestintheoceansmaydependonavarietyofprocessesincludingtheambientZnconcentrations,theextentofwatercolumnconsumption,andtheδ66Znofwaterssuppliedtotheeuphoticzone.However,wehavefoundthatkerogen(theinsolu-bleorganicfraction)andbitumen(thesolubleorganicfraction)ex-tractedfromcore-topsitesacrosstheCariacoBasin(seemethodsforfullextractiondetails)areallcharacterizedbyδ66Znvaluesthataremoredepletedthanambientwaters,providingclearevidencethat biological export sequesters isotopically depleted (light) Znwithinthesediments(Figure4).TheexportoflightorganicZnhas

F IGURE  3 ModernglobalisotopicmassbalanceofZn.(Top)fluxes.(Bottom)Isotopicrange.Thedashedlinerepresentsmeanδ66Znvalues(0.5‰)ofdeepseawater,andtheasterisksinbarshighlightthemeanδ66Znvaluesforthesesourcesandsinks.Fluxestimatesinroundbracketsare×108 mol year−1ofZn.SeeTableS1forfulllistofreferences[Colourfigurecanbeviewedatwileyonlinelibrary.com]

δ66Zn0.60.40.20 0.8 1.0–0.2–0.4–0.6

Riverine

Sources

Aeolian dust

1.2 1.4

Hydrothermal fluids

Sinks

Fe-Mn oxide

Carbonate

Euxinic precipitates

Organic biomass

Silica

Lithosphere

Organic delivered (62%)

Euxinicsediments (11%)

Ferromanganese crust (20%)

Silica (4%)

Carbonate (3%)

Rivers (92%)

Aeolian dust (8%)

Hydrothermal(<1%)

     |  345ISSON et al.

alsobeensuggestedinothermodernmarinesettingsbasedonZnisotopeanalysesinbulksediments(Littleetal.,2016).Inacriticalmanner,wealsoprovideevidenceforpreferentialburialofisoto-pically light organic Zn in ancient sedimentary rocks (i.e., δ66Znvalueslessthanseawaterinputsourcesofapproximately+0.33‰(Little,Vance,etal.,2014);Figure5b).Althoughtheisotopiccom-positionoforganicZninancientshalesoflowthermalmaturityisvariable,theseδ66Znorgvaluesareonaveragesignificantlylighterthantheassumedinputterms.Thus,theδ66ZnorgrecordprovidesclearevidencethattheorganicZnflux leadstoburialof isotopi-callylightZn.

Profilesforδ66Zninmodernmarinewatercolumnsdonottypi-callyincreasetowardthesurfacedespitetheexportoflightorganicZn from seawater (Conway& John, 2014; John& Conway, 2014;Zhao,Vance,Abouchami,&DeBaar, 2014). This apparent lackofan expressed biological fractionation in near-surface waters mayreflect a role forZn adsorption in controllingwater columnδ66Zn(John&Conway,2014;Köbberich&Vance,2017)(FigureS1).Zincis predominantly complexed by organic ligands, many with un-knownstructures,orsorbedtobiologicalormineralogicalsurfaces(Bruland,1989; Jakubaetal., 2012; John&Conway,2014; Lohan,Statham, & Crawford, 2002). Ligands preferentially complex theheavyisotope(Jouvin,Louvat,Juillot,Maréchal,&Benedetti,2009;Köbberich&Vance,2017;Markovićetal.,2016),leavingtheresidual

dissolvedZn2+poolisotopicallylight(John&Conway,2014).Ithasbeenproposed thatnatural phytoplankton communities alsohavetheabilitytoregulateambientZnconcentrationsinsurfacewatersviarapidligandproductiontoreduceZntoxicity,particularlywhereZnconcentrationsarehigh (Lohanetal.,2005).Theabundanceoforganic ligands has beenobserved to be closely linkedwith ratesofsurfaceproductivity (John&Conway,2014;Kozelka&Bruland,1998;Lohanetal.,2005;Wells,Kozelka,&Bruland,1998).Thesizeofthisorganicligandpoolcanbeextremelydynamic,withgenera-tionandremineralizationoccurringonthetimescaleofdays.Rapidoxidation of organic ligands in both surface waters and at depthreleases the ligand-bound Zn back into solution (John&Conway,2014;Lohanetal.,2005).Thelikelihoodofanygeologicallymean-ingfulligand-boundZnburialfluxisthereforelow.Thisassumptionisconsistentwithourdataset,whichindicatesisotopicallydepletedδ66Znorg relative to sulfideboundZn (δ

66Znsulf) across thebreadthofthegeologicalrecord(seebelow;Figure2).Insum,multiplepro-cessesgoverntheexpressionofZnisotopesinsurfacewaters,eachassociatedwithpotentiallylargeintrinsicfractionations.Watercol-umn isotopic profiles therefore express intricate spatial and tem-poralvariabilitythatcannotbeaccountedforbyanysingleprocess(e.g., uptake, sorption, remineralization), and future work will nodoubt continue tomove forward our understanding of Zn cyclingin theupperoceans.However,what is critical forourpurposes is

F IGURE  4 Znisotopedataofthesulfide,bitumen(TLE),andkerogen(HyPy)fractionsofeuxiniccore-topmudsfromninesitesacrosstheCariacoBasin.Themeanvalueofδ66Znsulf(+0.50±0.07‰2SD,n = 9)accuratelycapturestheglobaldeepoceanwaterδ66Znsignature(+0.50±0.14‰2SD,n = 223).Verticalerrorbarsdenoteexternalreproducibility.δ66Znorgvaluesareconsistentlymorenegativethanthoseofdeepseawater[Colourfigurecanbeviewedatwileyonlinelibrary.com]

Deep-Seawater

δ66Z

n

(1) (2) (3) (4) (5) (6) (7) (8) (9)

SulfideOrg (Bitumen, TLE)Org (Kerogen, HyPy)

1.0

100

1,400

1300900

700500300

900

300

300

500

700900

1,1001,300

500

10030011ºN

10ºN 66º 65º

Margarita

Cubagua

Araya

Cumana

Piritu

Unare platform

Rio Unare

Laguna de Tacarigua

Rio Tuy

Cabo Codera

Tortuga

Tortuga Bank

Venezuela

0 500

km

N

E

1

23

456

7

89

0.8

0.6

0.4

0.2

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346  |     ISSON et al.

thattheisotopiccompositionoftheburialfluxesultimatelycontrolsthemeanvaluesforglobalanddeep-waterdissolvedδ66Znandthatmodern and ancient sedimentaryorganicmatter (Figures4 and5)areisotopicallydepleted.

Sulfide capture is particularly important to our discus-sion because of our emphasis on shale-hosted isotopic data. Atdepths >100–300m in the modern oceans, the isotopic compo-sition and concentration of dissolved Zn are largely homogenous(+0.50±0.14‰2SD,n = 223;Bruland,1980;Conway&John,2014;

Conway&John,2015;Jakubaetal.,2012; John&Conway,2014;John,Helgoe,&Townsend,2017;Zhaoetal.,2014).Hence,tempo-ralvariationsintheisotopicsignatureofthedeep-seareservoircanthereforeshedlightonchangesintheglobalbiogeochemicalcyclingofZn.Here,weprovidenewdataindicatingthatcaptureofZnineu-xinicsedimentscanserveasaseawaterarchivebasedonanalysisofsedimentsfromtheCariacoBasin.TheCariacoBasinispermanently(ratherthanseasonally)euxinic(anoxicandsulfidic)andZnprecipi-tatesoutofsolutioneitherasauthigenicZnsulfidesorbyscavenging

F IGURE  5 SedimentaryZnisotoperecordspanning3.5billionyearsofEarth’shistory.(a–b)Newdatafromthesulfide(bluecircles),bitumen(redcircles)andkerogen(blacksquares)fractionsofsulphidicblackshales(n = 502).HorizontalgrayfieldsdenotethecrustalZnisotopicrange(32).Verticalerrorbarsdenoteexternalreproducibility.Weidentifythreestageswithinthesulfiderecord.Stage1(pre-800Ga):sulfidesexpressrestrictedvalueswithinthecrustalrange.Stage2(lateNeoproterozoic):transitionintervalduringwhichδ66Znsulf valuesdistinctivelylighterandheavierthanthecrustalrangeareexpressed,likelyreflectingboththeecologicalriseofeukaryotesand re-organizationoftheglobalbiogeochemicalZncycle.Stage3(Phanerozoic):isotopicallylightδ66Znsulfvaluesareabsent,andmeanvaluesaredistinctivelymorepositivethanthoseofthecrustalaverage.(c)Frequencydistributionsofbootstrapresampledmeansofsulfide(blue)andorganic(bitumenandkerogen)(red)Znisotopedatapre-andpost-800Ma[Colourfigurecanbeviewedatwileyonlinelibrary.com]

2.0 1.01.5 0.5 03.0 2.5

Age (Gyr Ago)

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0.5 01.01.5

Stage 1 Stage 2 Stage 3

     |  347ISSON et al.

duringironsulfideprecipitation(Morse&Luther,1999).Sulfidescanalso capture organic-delivered Zn released during biomass decaywithinsedimentaryporewaters,aprocessthatwoulddrivethesig-nature toward lighter δ66Zn values typical of organicmatter. Zincsulfide formation can also be associated with a negative isotopefractionation (Vance etal., 2016). However, near-quantitative Zndrawdown,duetomuchlowerZnconcentrationrelativetothatofH2S,asistypicalinsulfide-richwatercolumnsandporewaters(e.g.,Tankéréetal.,2001), is likelytomute isotopefractionationtiedtoaqueous Zn speciation or kinetic effects during sulfide precipita-tion(John,Kunzmann,Townsend,&Rosenberg,2017;Vanceetal.,2016).Consistentwithmuted fractionationsduring sulfide forma-tion,wefindthatδ66Znvaluesforauthigenicsulfidefromcore-topsitesacross theCariacoBasin (+0.50±0.07‰;Figure4)are indis-tinguishable from the globally homogenous δ66Zn in the moderndeepocean (+0.50±0.14‰,n = 223).AsAtlanticdeepwatersarethemain source of Zn into theCariacoBasin, these observationssupportthatthereislimitednetisotopicoffsetfromseawaterduringZnsulfideburial.Buildingon theseobservations,wepropose thatsulfideswillnotbeamajor lever indrivingchanges inthe isotopiccompositionofseawater.Insum,sulfidesinblackshalesdepositedinancientanoxicsettingscanprovidearobustrecordofdissolvedδ66Znvaluesforseawaterasithasevolvedovergeologictime.

WithinthisglobalZnisotopemassbalanceframework,theburialofisotopicallylightZntiedtobiologicaluptakeisthecentralprocessthatcandrivetheglobalseawaterδ66Zntovaluesthataremoreposi-tivethantheinputs(Figure3).Thisframeworkbuildsfromthemech-anismscontrollingZnburialandallavailablesedimentaryZnisotopedata(seebelow).Assumingthatthereisnotemporalvariationintheδ66Znof inputs, positive shifts inmean seawaterδ66Znvalues canthusbecausedby(i)anincreaseintheamountofisotopicallylightor-ganicburialand/or(ii)alargernetisotopicfractionationforbiologicalZnuptakedrivenbygreaterZnbioavailability.Wefindthatthefrac-tionationfactorassociatedwithorganicZnburial (Δ66Znorg-diss)canbeestimatedtoruleoutoption(2),makingitpossibletouseZniso-topestoquantitativelytracktheevolutionofeukaryoticorganiccar-bonexportasaresultoftheirsignificantlyelevatedZnrequirements.

4  | ZINC ISOTOPE SYSTEMATIC S THROUGH TIME

WepresentanextensivenewZnisotoperecord(n = 502)fromalargesamplesetoforganic-richblackshalesspanningfromtheArcheantothepresent(Figure5),withtheaimofusingtheδ66Znsulfrecordtotrackseawaterevolutionandorganic-boundZntoestimatetheiso-topicoffsetbetweenorganicmatterandcoevalseawater(Δ66Znorg-

sulf) through time. In a specific manner, these data encompass acomprehensiverecordofleachedsulfidephases(δ66Znsulf)frompre-viously examinedblack shales from65 formations (Figure5a).Wefocusedonsulfidicshales,whichhaveahighpotentialforcapturinggloballyhomogenousdeepseawatervalues(seeabove).Priortothemid-Neoproterozoic(~800Ma),thesulfidefractionintheexamined

blackshalesshowsδ66Znvaluesindistinguishablefromthoseofthepresumed input sources (mean +0.33‰, range +0.17 to +0.58‰;Figures5,S4–S5).Thefirstdatawellaboveassumedinputvaluesarefoundinthe~800MaWynniattFormationoftheShalerSupergroupinArcticCanada(δ66Znsulf>0.9‰)(Thomson,Rainbird,Planavsky,Lyons,&Bekker,2015) (Figure5,S5).Thesepositiveδ66Znsulf val-ues remainprevalent throughout the lateNeoproterozoic and thePhanerozoic.Variabilityinδ66Znsulfvaluesafter~800Macanbetiedtoshiftsineitherglobaldeepwater,localseawater,orvaryingpore-watersignalsthatoverprinttheglobalsignal.Nonetheless,theonsetofpositiveδ66ZnsulfvaluesrecordsafundamentalshiftintheglobalZncycle.Weproposethatthisshift inglobalZnisotopecyclingat~800Mamarksanincreaseintheburialoforganic-derivedZn,prin-cipally as eukaryoticbiomass, rather than changes in global redoxconditionsorZnbioavailability(seeSupplementaryInformationandbelowfordiscussion).

OxygenationthroughtheNeoproterozoicwas likelyprogressive(e.g.,PoggevonStrandmannetal.,2015),andthisoxygenationwouldhavereshapedtheZncycle.Specifically,theburialofZnassociatedwith oxides is an important component of themodern Zn isotopebudget,andthisfluxwouldhaveincreasedwithoceanoxygenation.OxideboundZnburialwaslikelyreducedinlargelyanoxicoceans.AsoxideburialisassociatedwithapositiveZnisotopeeffect,Zn-metaloxideburialoughttodecreaseratherthanincreasedissolvedseawa-terδ66Znvaluesandthereforecannotexplaintheobservedshiftat~800Ma.Incontrast,moreoxicconditionswouldhaveledtoacor-respondingdecreaseinsulfideburialoncesulfateburialinanincreas-inglywell-oxygenatedoceanbecameprevalent.Further,althoughtheratioofwatercolumntoporewatersulfideburialmayhavedecreasedwithoceanoxygenation,Zncapturewithinbothporewatersandeu-xinicwatercolumnsislikelytobenearquantitativeandthusanypos-sible(intrinsic)Znisotopefractionationduringsulfideformation(e.g.,Vanceetal.,2016)isunlikelytobeexpressed.

VariationsinaqueousZnspeciationmayalsobeexpectedwithashift inoceanredoxchemistry.Foremost,marinesulfate levelshaveincreaseddramaticallythroughoutEarth’shistorytrackingincreasingoxygenationandoughttohaveincreasedatleasttransientlyataround800Ma (Turner&Bekker,2016).However, a rise in sulfate levels isunlikelytoexplaintheobservedisotopictrendsgiventhatZn-sulfatecomplexes are weak andmake-up a negligible component (<6%) ofmarineZnspeciestoday(Black,Kavner,&Schauble,2011;Fujiietal.,2014),despitemarinesulfatelevelsthatarecurrentlyattheirhighestpointinEarth’shistory(Canfield&Farquhar,2009).Inadditionevenifpresent,ab initiocalculationspredict limited isotopicfractionationassociatedwiththeformationofZn-sulfatecomplexes(Fujii,Moynier,Pons,&Albarède,2011).Thus,oceanoxygenationislikelytohavehadasignificanteffectontheglobalZncycle,butthisprocessisunlikelytohavedirectlydriventheobservedshifttomorepositiveδ66ZnsulfvaluesintheNeoproterozoicthroughoxide-orsulfideburial-relatedcontrols.

ThebioavailabilityofZn inseawaterhasthepotential to influ-encetheZnisotopefractionationassociatedwithbiologicaluptake.LowlevelsofZnbioavailabilityinProterozoicoceanswerepreviouslyproposedbasedonthermodynamicconsiderations(Saito,Sigman,&

348  |     ISSON et al.

Morel,2003),andlowZnbioavailabilitycouldinprinciplehavere-sultedinmutedΔ66Znorg-swvaluespriorto~800Ma.However,thismodelhasrecentlybeenchallengedbasedonrecordsofapprecia-blesedimentaryZnenrichmentduringthisinterval(FigureS3)andthus ample supplies in seawater (Robbins etal., 2013; Scott etal.,2012).OurZnisotopedatasetsupportsthelatterview.Specifically,weobservenearconstantΔ66Znorg-sulfvaluesofabout−0.36‰priorto~800Ma(Figure5), indicatingthatburialofisotopicallylightZnwithorganicmatteroccurredpriortothemid-Neoproterozoicrisein δ66Znsulfvalues.Therefore, the lightZn isotopevaluesrecordedintheorganicfractionofshalesindicatethattheobservedshiftinδ66Znsulf(i.e.,ourproxyforcoevalbottomwaters)isalsounlikelytobelinkedtoashift inZnisotopefractionationduringorganicmat-ter uptake and burial. We observe a subtle shift toward smallermean Δ66Znorg-sulfvaluesafter~800Mafrom−0.36‰to−0.26‰(Figure5c),whichwould,ifanything,mutetheobservedincreaseinδ66Znsulf.

TheobservedtrendinorganicZndataisunlikelytoreflectapat-ternofalteration,becauseonlystrataoflowthermalmaturitywithnodiscerniblecontaminationwereselectedforδ66Znorganalysis(oilwindowmaturity or lower based on Rock-Eval pyrolysis and lipidbiomarkerdata;seeSupplementaryInformation).Thereforewecon-cludethatlightorganicZnwasbeingdeliveredtothesedimentpilethroughtheProterozoic,buttheextentoforganic-derivedZnburialwaslikelytoolowtodriveseawatertosignificantlyheavyδ66Znval-uespriorto800Ma.ThismodelisconsistentwithanobservedjumpinorganicZnconcentrationsinthemid-Neoproterozoic(byoveranorderofmagnitude in termsofbootstrap resampledmeanvalues;Figure6).

Wefindthatthemostparsimoniousexplanationfortheobservedmid-Neoproterozoic-Phanerozoicriseinmarineδ66Znisanincreaseinorganic-derivedZnburial,givenevidenceforthenearlyconstantΔ66Znorg-sulfvalues,anexpecteddecreaseindeepoceanδ

66Znwithocean oxygenation via removal of 66Zn onto metal oxides, and asmallersulfidesinkforZn.WeproposethatthistransitionwasmostlikelycausedbybothahigherZndemandfollowingtheriseofeu-karyotestoecologicaldominanceinphasewithanoverallincreaseintotalglobalproductivity.WefindinourZnisotopemassbalancethatanincreaseinorganiccarbonburialaloneisinsufficienttoaccountfor

thepositiveZn isotopevaluesobserved inpost-800MasedimentsifburiedwiththeZn/Cratioweobserveforpre-800Masedimen-taryorganicmatter(Figure7).Rather,wefindthatincreasesinma-rineorganicZn/Careessentialtodrivetheobservedriseinseawater

F IGURE  6 Frequencydistributionsofbootstrapresampledmeansoforganic(bitumenandkerogen)Znabundancedata,aspresentedinFigure5,pre-(black)andpost(gray)-800Ma[Colourfigurecanbeviewedatwileyonlinelibrary.com]

0 100 200 300 400 500 600 700 800 900 1,0000

200

400

600

800

1,000

1,200

1,400

Post-800 Ma

Pre-800 Ma

Organic [Zn] (ppm)

F IGURE  7 GlobalZnisotopemassbalanceforapre-andpost-800Maocean,illustratingdeviationsintheZnisotopiccompositionofseawaterawayfrommeansourceinputvalues(verticalaxis),withgivenchangesin(1)organiccarbonburial(horizontalaxis)and(2)theZn/Cratiooforganicbiomassbeingexported(dashedandsolidlines).Blacklinesrepresentmodernoxicremovalflux(1.7×108 mol yr−1),andredrepresentscalculationsforapervasivelyreducingoceaninwhichthereisnegligibleoxicburial.Weadoptabiologicalisotopefractionationfromseawater(Δ66Znorg-sw)of−0.5‰,andariverineinputfluxof13×10

8molesyr−1.OurmodelingsuggeststhatthattheZnisotopecompositionofseawaterislargelyinsensitivetoasystemlargelycharacterizedbyprokaryoticcells(Zn/Cratioof~10).ThismodelsuggeststhatmuchlargerZn/Cratiosof~100,typicalofeukaryoticphytoplankton,arerequiredforanyoceansystemtoachieveδ66Znvaluesthatare0.5–0.7‰greaterthanthesourcemean,afeatureofpost-800Maseawater.Anincreaseinorganic-derivedZnburialacrossthemid-Neoproterozoicsuggestsafundamentalrestructuringofglobalmarineecosystemstructures,towardamoreeukaryote-richsysteminwhichthereismoreextensivebiologicalZnutilization(FigureS2)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

0 2 4 6 8 10 12–0.2

–0.1

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

Global organic carbon burial (Tmol yr–1)

∆66

(‰

)sw

-inp

ut

Biomass Zn:C1005010

Increasing Zn:C

Stage 1(Pre-800 Ma)

Stage 3(Phanerozoic)

     |  349ISSON et al.

δ66Zn(Figure7).ThisframeworkisconsistentwiththeobservedlateNeoproterozoic to Phanerozoic increase in organic Zn concentra-tions (Figure6).Wepropose that theobserved rise in sedimentaryorganicZn/Cislikelylinkedtoalargereukaryoticcontribution(withanelevatedZn/Cratio)toexportedmarinebiomass.Moreover,ourfirstmarkedlypositiveZnisotopevaluesappeararound800Ma,butadditionalworkintheNeoproterozoicandPhanerozoicisneededtodetermineiftheNeoproterozoicZncycleoscillatedbetweentypicalmid-ProterozoicandlateNeoproterozoic/Phanerozoicstatesasop-posedtoasinglestatechange.

5  | CONCLUSION

Given fossil evidence for eukaryote emergence at > ~1700Ma(Butterfield,2015;Knoll,2014;Parfrey,Lahr,Knoll,&Katz,2011),ourZnrecordsprovidesupportforalong(billon-year)lagbeforetheirrisetoecological prominence at~800Ma,which is consistentwith theearliestrobustfindingofdetectablesteranecompoundsinthermallywell-preservedsedimentaryrocks(Brocksetal.,2017).Thissteranebiomarker signalwas attributed tomainly unicellular heterotrophicprotists,asgaugedfromtheunusualC27steranecarbonnumberdom-inance(Brocksetal.,2017),butsubstantialcontributionsfromeukar-yoticphytoplankton(inparticularfromredalgalclades)couldproducesimilarsteranepatterns(Kodner,Pearson,Summons,&Knoll,2008)andaccountforsomeappreciablesterane/hopaneratios(0.003–0.42reportedforasmall720–820Masampleset)(Brocksetal.,2017).Inaddition,theZnrecordprovidesanopportunitytoevaluatetheimpactthatthefirstabundanteukaryoticexportproductivitymayhavehadonNeoproterozoic climatic and carbon cycleperturbations. For in-stance,theshiftinecosystemstructurerecordedinourisotopicdataoccurredalmost80millionyearsbeforetheonsetofthe“SnowballEarth”eventschallengesprevioussuggestionsthatalgalproliferationwasintimatelyanddirectlylinkedwiththeonsetofglaciation(Feulneretal.,2015;Tzipermanetal.,2011).Atthesametime,theincreaseineukaryotecontributiontoprimaryproductivitycoincidedwithadra-maticshifttowardmoredynamiccarbonisotopevaluesinmarinecar-bonatesfollowingmorethanabillionyearsofrelativeδ13Cstability,andjustpriortothefirstappearanceofmicrofossilsfortestateamoe-bae(eukaryoticheterotrophs)(Porter&Knoll,2000),markingtheendofanextendedbiogeochemicalstasisthatprevailedinthepreceding“boringbillion”.WhileestablishingthecauseandeffectrelationshipsbehindtheseobservationsviamoredetailedNeoproterozoicrecordsremainsimportantforfutureresearch,theZnisotoperecordnever-theless suggests that the proliferation of eukaryotes in the oceanswas closely coupledwith the onset of dynamic environmental andbiogeochemicalevolutionduringthemid-Neoproterozoic.

ACKNOWLEDG MENTS

The authors acknowledge funding from the NSF FESD Program(TL, GL) and the NASA Astrobiology Institute under CooperativeAgreementNo.NNA15BB03AissuedthroughtheScienceMission

Directorate (TL, CD,CR,GL,NP, etc.).We are extremely gratefultoAndyKnoll,LarryPetersonandChristopherJuniumforprovidingsamplesforthisstudy.

ORCID

Terry T. Isson http://orcid.org/0000-0002-1040-0230

Alan D. Rooney http://orcid.org/0000-0002-5023-2606 Eva E. Stueeken http://orcid.org/0000-0001-6861-2490

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How to cite this article:IssonTT,LoveGD,DupontCL,etal.Trackingtheriseofeukaryotestoecologicaldominancewithzincisotopes.Geobiology. 2018;16:341–352. https://doi.org/10.1111/gbi.12289